Global phylogenomic analysis of nonencapsulated Streptococcus pneumoniae reveals a deep-branching classic lineage that is distinct from multiple sporadic lineages

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Hilty, Markus
Wuethrich, Daniel
Salter, Susannah J
Engel, Hansjuerg
Campbell, Samuel
Sa-Leao, Raquel
de Lencastre, Herminia
Hermans, Peter
Sadowy, Ewa
Turner, Paul
Chewapreecha, Claire
Diggle, Mathew
Pluschke, Gerd
McGee, Lesley
Eser, Ozgen Koseoglu
Low, Donald E
Smith-Vaughan, Heidi
Endimiani, Andrea
Kueffer, Marianne
Dupasquier, Melanie
Beaudoing, Emmanuel
Weber, Johann
Bruggmann, Remy
Hanage, William P
Parkhill, Julian
Hathaway, Lucy J
Muehlemann, Kathrin
Bentley, Stephen D
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2014
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Abstract

The surrounding capsule of Streptococcus pneumoniae has been identified as a major virulence factor and is targeted by pneumococcal conjugate vaccines (PCV). However, nonencapsulated S. pneumoniae (non-Ec-Sp) have also been isolated globally,mainly in carriage studies. It is unknown if non-Ec-Sp evolve sporadically, if they have high antibiotic nonsusceptiblity rates and a unique, specific gene content. Here, whole-genome sequencing of 131 non-Ec-Sp isolates sourced from 17 different locations around the worldwas performed. Results revealed a deep-branching classic lineage that is distinct frommultiple sporadic lineages. The sporadic lineages clustered with a previously sequenced, global collection of encapsulated S. pneumoniae (Ec-Sp) isolates while the classic lineage is comprised mainly of the frequently identified multilocus sequences types (STs) ST344 (n =39) and ST448 (n=40).All ST344 and nine ST448 isolates had high nonsusceptiblity rates to b-lactams and other antimicrobials. Analysis of the accessory genome reveals that the classic non-Ec-Sp contained an increased number of mobile elements, than Ec-Sp and sporadic non-Ec-Sp. Performing adherence assays to human epithelial cells for selected classic and sporadic non-Ec-Sp revealed that the presence of a integrative conjugative element (ICE) results in increased adherence to humanepithelial cells (P= 0.005). Incontrast, sporadic non-Ec- Sp lacking the ICE had greater growth in vitro possibly resulting in improved fitness. In conclusion, non-Ec-Sp isolates from the classic lineage have evolved separately. They have spread globally, are well adapted to nasopharyngeal carriage and are able to coexist with Ec-Sp. Due to continued use of PCV, non-Ec-Sp may become more prevalent.

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Genome Biology and Evolution

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6

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12

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© The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

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Biochemistry and cell biology

Evolutionary biology

Evolutionary biology not elsewhere classified

Genetics

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